Palynological study of carbonated mounds during the holocene along the atlantic and mediterranean moroccan margins

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Palynological

Study of Carbonated Mounds during the Holocene along

the

Atlantic and Mediterranean Moroccan Margins

Jihad

Rachid

a,

⁎

, Touria Hssaida

a

,

Naima Hamoumi

b

,

Loubna Terhzaz

b

,

Silvia Spezzaferri

c

,

Norbert

Frank

d

,

Lamia Daghor

e

a _{Hassan II University, Laboratory dynamics of sedimentary basins and geological correlations, Faculty of Sciences Ben M'Sick Casablanca, Morocco}

b _{Mohammed V University, Research Group ODYSSEE Laboratory Materials, Nanotechnology and Environment (LMNE), Research Center for Materials Science, Faculty of Sciences Rabat,}

Morocco c _{University of Fribourg, Dpt. Geosciences, B.1700 Fribourg, Switzerland}

d _{Heidelberg University, Institute of Environmental Physics and Institute for Geosciences, Heidelberg, Braden-Württemberg, Germany}

e _{Laboratory of Ecology and Environment, Department of Biology, Faculty of Sciences Ben M'sik, Hassan II University of Casablanca, B.P. 7955, Sidi Othmane, Casablanca, Morocco}

a b s t r a c t

Keywords: Palynology Dinoﬂagellate cysts Carbonated mound Holocene

Atlantic and Mediterranean Moroccan margins

A palynological study of carbonate mounds of Atlantic and Mediterranean Moroccan margins was conducted on sediment boxcores MD13-3441, MD13-3456, MD13-3461, MD13-3465, MD13-3468 collected during the ocean-ographic cruise MD 194/Euroﬂeet - GATEWAY, which took place on June 2013.

The organic remaining revealed a dominance of dinoﬂagellate cysts over the continental fraction, which showed very low rates. The use of pollen data, despite their low representativity, is proving to be a valuable tool for the paleoclimate interpretation.

The palynological quantitative and qualitative analysis revealed the evolution of the paleoenvironment and cli-mate change of the carbonate mounds during this study interval. The terminal Pleistocene–basal Holocene pas-sage highlighted by the dominance of cold taxa of dinoﬂagellate cysts. The presence and dominance of tree and shrub pollen coupled by the presence of altitudinal conifers conﬁrmed a cold climate in both continental and ma-rine environments.

During the lower-middle Holocene, the variations in the relative frequencies of dinoﬂagellate cyst associations reﬂect the evolution of the paleoenvironment from inner neritic to oceanic.

The recorded microﬂora shows a cyclicity during the lower Holocene from arid to semi-arid between 10.07 and 9.85 ka (the abundance of herbaceous and steppe), to become arid again around (9.69 ka) by the consistently high rate of herbaceous and steppe.

In contrast, the paleoclimate recorded during the Middle Holocene is semi-humid to 6.29 ka (high rate of trees and shrubs) and evolves to a warm dry climate at 5.9–5.14 ka, reﬂected by the abundance of herbaceous and steppe.

1. Introduction

Since their discover along the European Atlantic margins, cold-water carbonate mounds stimulated the interest of many researchers.

Cold water coral mounds along the Moroccan Atlantic margin (Gulf of Cadiz) were discovered for the_{ﬁrst time during the oceanographic}

cruise CADIPOR I Belgica 02/12 in 2002 (Van Rooij et al., 2002) and along the Moroccan margin of the Eastern Mediterranean (Alboran Sea), during the oceanographic cruise R/V Hesperides in 2006 (Comas and Pinheiro, 2007).

The Beta carbonate mound on the Moroccan North Atlantic margin was investigated for sedimentology and stable isotope (oxygen and car-bon) byDe Mol et al. (2011, 2012),Terhzaz (2019),Fink et al. (2013),

Titschack et al. (2016)andTerhzaz et al. (2018)studied the sedimentol-ogy and geochemistry of the sediments recovered on the Brittlestar I ridge and Cabliers Mound along the Moroccan Mediterranean margin. Benthic foraminiferal and ostracod assemblages were related to the cir-culation patterns and marine productivity in the Alboran Sea (Fink et al., 2013; Stalder et al., 2015, 2018, 2019). Age constrain for corals, benthic

⁎ Corresponding author.

E-mail addresses:rachidjihad231@gmail.com(J. Rachid),touria.hssaida@gmail.com

(T. Hssaida),naimahamoumi5@gmail.com(N. Hamoumi),loubna.terhzaz@gmail.com

(L. Terhzaz),silvia.spezzaferri@unifr.ch(S. Spezzaferri),

norbert.Frank@iup.uni-heidelberg.de(N. Frank),l.daghor@gmail.com(L. Daghor).

http://doc.rero.ch

Published in "Review of Palaeobotany and Palynology 278(): 104213, 2020"

which should be cited to refer to this work.

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foraminifera and associated fauna through time was proved byAguilar et al. (2013),Fink et al. (2013)andStalder et al. (2015, 2018, 2019).

A palynological (pollen and dinoﬂagellate) investigation to recon-struct the impact of marine and terrestrial climate changes on carbonate mounds and cold-water corals ecosystem was missing until now.

Dinoﬂagellates are planktonic organisms include that can be divided into autotrophic, using only photosynthesis and heterotrophic using dif-ferent energy sources. Autotrophic dinoﬂagellates have latitudinal dis-tribution (Wall et al., 1977; Harland, 1983; Edwards and Andrle, 1992) which is controlled by temperature and salinity of surface waters, marine circulation patterns and nutrient supply (Dale, 1976; Eynaud et al., 2004; Harland, 1983; Morzadec-Kerfourn, 1988; Taylor and Pollingher, 1987; Turon et al., 2003; Wall et al., 1977; Zonneveld et al., 2013). They are generally used as an indirect measure of primary pro-ductivity of ocean waters (Turon and Londeix, 1988; Devillers and de Vernal, 2000). Their cysts have proven to be excellent bioclimatic tracers in the Quaternary (Turon, 1984).

This research is part of the international programs“Cold-water car-bonate mounds in shallow and Deep Time” (COCARDE). It presents the results of the palynological study of Box cores: MD13-3441, MD13-3456, MD13-3461, MD13-3465 and MD13-3468 retrieved in the North Atlantic off Morocco (Gulf of Cadiz) and the Alboran Sea on the Brittle Star I ride off Melilla during the oceanographic cruise MD 194, EURO Fleet Gateway-TORE aboard the N / O Marion Dufresne held from 10 to 21 June 2013.

2. Geological setting, geodynamic and oceanographic 2.1. Geological setting

The Gulf of Cadiz is located in the northeastern part of the Atlantic Ocean between Africa and Europe, between 37° parallel North and 34° latitude south and between meridians 6 ° and 9 ° West. It extends west of the Gibraltar Strait to the south of Cape St. Vincent, along the Portuguese and Spanish margins (Mulder et al., 2002, 2003; Hanquiez, 2006; Marchès et al., 2007; Hanquiez et al., 2010). This complex geolog-ical setting is bounded to the north by the transform fault Azores-Gibraltar and to the east by the arc of Azores-Gibraltar (Maldonado et al., 1999; Medialdea et al., 2004, 2009; Zitellini et al., 2009).

It evolved from passive margin into an active margin from the Meso-zoic to the early CenoMeso-zoic, then into a fore arc during the lower Miocene andﬁnally to a passive margin with a subsiding basin in the late Mio-cene (Maldonado and Nelson, 1999).

Tectonic activity is responsible for the irregular topography of the seaﬂoor in this region, characterized by banks, diapirs, ridges and mud volcanoes (Maldonado et al., 1999; Kenyon et al., 2000). Locally cold-water carbonate mounds hosting cold-cold-water corals are also present in this region (De Mol et al., 2012).

The Alboran Sea is the western part of the Mediterranean Sea, it has a maximum depth of 2 km, a length of 400 km and a maximum width of 200 km. It is limited to the north by the Betic Chain of Spain, to the south by the Rif Mountains in Morocco and Tell Algeria Chain, to the west by the Strait of Gibraltar and to the east by the line connecting Cape Figalo in Algeria in the Cabo de Gata in Spain (Carter et al., 1972).

The Moroccan Alboran margin consists of a continental shelf (0–200 m depth) rather narrow, with a width around 5 km opposite to the three Forks Cape, around 16 km from its central portion, opposite to the Bay of Nador. This platform shows a gentle and regular slope with isobaths parallel to the shore between 0 and 45 m, but it ends with a sharp slope towards the south Alboran basin (Tesson and Gensous, 1979).

The tectonic setting of the Alboran basin results from the post-Messinian deformation. In the Holocene, the transtensive tectonics has generated new depocentres and transpressional tectonics has gener-ated local uplifting positive structures such as the Alboran Ridge (Comas et al., 1999). The evolution of the Alboran basin is characterized

by the accumulation of sediments and a calc-alkaline to alkaline magmatism (Comas et al., 1999). The Alboran Sea shows a complex to-pography with several sub-basins, ridges, banks and mounds. 2.2. Oceanographic setting

The present day oceanographic circulation in the Gulf of Cadiz is con-trolled by the exchange of water through the Strait of Gibraltar. Surface Atlantic water masses (AIW)ﬂow into the Alboran Sea, and the deep water Mediterranean masses (MOW)ﬂow into the Atlantic Ocean (Lacombe and Lxzeray, 1959; Ochoa and Bray, 1991; Nelson et al., 1999; Hanquiez, 2006).

Five water masses characterize the southern Gulf of Cadiz: the North Atlantic surface waters between 0 and 200 m, the North Atlantic central water masses between 200 and 600 m, the intermediate Antarctic wa-ters masses between 600 and 1500 m. Mediterranean wawa-tersﬂow at around 1000 m of water depth and the deep North Atlantic masses wa-tersﬂow below 1500 m (Machín et al., 2006; Ambar et al., 2008; Louarn and Morin, 2011).

The Alboran basin is a transition region between two water bodies: the Atlantic Ocean and the Mediterranean Sea. Four water masses can be identified in the Alboran Sea: the Atlantic Water (AW) from the sur-face to 150 m of water depth, the Atlantic modified water (MAW) at 150–200 m water depth flow through the Strait of Gibraltar to the Algeria Basin; the Levantine intermediate water (LIW)flow between 200 and 600 m, are formed in the eastern Mediterranean Sea and the flow west to the Atlantic Ocean; the West Mediterranean deep water (WMDWs) are present below the LIW formed in the Gulf of Lions in the northern part of the West Mediterranean Sea (Benzohra and Millot, 1995).

Two semi-permanent gyres (eddies) are formed after the inlet of North Atlantic Water Surface through the Strait of Gibraltar and their development is controlled by several factors such as atmospheric pres-sure, temperature, salinity (Heburn and La Violette, 1990; Vargas-Yáñez et al., 2002).

2.3. Climate context

The present climate along the Moroccan North Atlantic margin is oceanic and temperate; it is sub-humid, with hot and cool Summers, and cold and humid Winters according to the index of Martonne. The climate in the Moroccan Mediterranean margin is typically Mediterra-nean with contrasting seasons and local microclimates inﬂuenced by al-titude and Saharian inﬂuences. According to the index of Martonne, it is semiarid temperate or warm winter (Barathon, 1987b; Bouslam, 1989). The dominant wind directions is SW in Summer and WSW in Winter (Barathon, 1987a) sometimes characterized by violent storms.

During the Quaternary, these regions experienced glacial and inter-glacial cycles that have resulted in the alternation of arid and humid pe-riods with abrupt transitions on the continent (Biberson, 1971; Wengler et al., 1992; Linstädter and Zielhofer, 2010).

3. Palynological analysis of sediments associated with carbonates mounds

3.1. Material and method

The studied sediments collected during the oceanographic cruise MD 194 EURO GATEWAY Fleet aboard the R/V Marion Dufresne, which took place from June, 10 to June 21, 2013 in the Atlantic and Med-iterranean Moroccan margins (Fig. 1,Table 1).The carbonate mounds sampled are:

- Beta mound (MD13-3441) in the North Atlantic Moroccan margin at 35° 17.765′N, 6° 47.276′W and 532 m of water depth,

- Brittlestar I Ride is (MD13-3456) in the Mediterranean Moroccan

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margin at 35° 26.19 N, 30.80 W 2 and 330 m of water depth, - Brittlestar I Ride Summit (MD13-3461) in the Mediterranean

Mo-roccan margin at 35° 26.53 N, 31.07 W 2 and 320 m of water depth, - Brittlestar I Ride West (MD13-3465) in the Mediterranean

Moroc-can margin at 35° 26.06 N, 30.85 W 2 and 346 m of water depth, - Near the Brittlestar I ride (MD13-3468) in the Mediterranean

Mo-roccan margin at 35° 25.91 N, 30.86° 2 and 470 W m water depth.

Twenty-eight samples were collected from different sediment types according to the shipboard description of box cores (Van Rooij et al., 2013). They were investigated for their palynological content in the lab-oratory of Micropaleontological analysis at the Faculty of Sciences Ben M'sik, Casablanca, according to the standard method requiring a chem-ical treatment with HCl (10%) and HF (40%) (for 24 h), sieving at 10μm and mounting the organic residue on the smear slide.

Fig. 1. Location of the studied cores (Table 1) in the Western Mediterranean and North-West Atlantic.

Table 1

General and geographical information concerning the 5boxcores of this study.

Mound Location Latitude (°N) Longitude(°W) Water depth (m)

Beta mound (MD13-3441) Gulf of Cadiz 35°17,75 6°47,28 −503

Brittlestar I Ride (MD13-3456) Alboran Sea 35°26,19 2°30,80 −330 Brittlestar I Ride Summit (MD13-3461) Alboran Sea 35°26,53 2°31,07 −320 Brittlestar I Ride West (MD13-3465) Alboran Sea 35°26,06 2°30,85 −346 Near the Brittlestar I ride (MD13-3468) Alboran Sea 35°25,91 2°30,86 −470

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Palynofacies were reconstituted based on assemblage composition: organic microfossils (pollen, spores, organic remains of foraminifera after the dissolution of the calcitic test, dinoflagellate, acritarchs) and algae. All palynomorphs were counted, but only dino_{flagellate cysts,} which are a reliable tool for reconstructions of Quaternary marine paleoenvironments, were counted at specific level. Specimen counting was performed using a Leica microscope with a natural light X40 mag-nification. Two hundred individuals were identified and counted per each slide to obtain statistically valid results. Less abundant and/or ac-cessory species were also considered to evaluate biodiversity. 3.2. Results

3.2.1. The Moroccan Atlantic margin

3.2.1.1. Box coreMD13-3441(from base to top):. Box core MD 13-3441 contains 90 cm of sediments. From the base to 85 cm they consist of brownish to grayish micritic mud, 85–65 cm and 55–35 cm contain brownish to grayish muddy micrite, 65–55 cm consist of brownish to grayish micritic mud, 35–25 cm and 15–0 cm contain of brownish to grayish muddy allochem limestones and from 25 to 15 cm consist of grayish allochemic mud (Terhzaz, 2019).

Eleven samples were processed for this box core. Their age span the interval between 12.09 and 6.8 ka before the present (Fig. 2) based on the age of the surrounding coral (Schröder-Ritzrau et al., 2015). Samples 90–75 cm correspond to the late Pleistocene/Tarentian (12.09–11.7 ka), from 75 to 25 cm to the lower Holocene/Greenlandian (11.70–10.9 ka), 25–15 cm in the middle Holocene/Northgrippian (10.84–7.43 ka) and above 15 cm surface the middle Holocene/Northgrippian

(7.43_{–6.8 ka). The stratigraphic placement takes into account the recent} ratiﬁcation of these stages and their limits by the International Subcom-mission on Quaternary Stratigraphy (ISQS) (a subcomSubcom-mission of the In-ternational Commission on Stratigraphy_{– ICS) being set Cambridge on} June 19, 2018. At 11,700 (before AD 2000). Tarentian/Greelandian, 8326(before AD 2000).Greelandian/Northgrippian 4250 (before AD 2000), Northgrippian/Meghalayian.(Walker et al., 2018).

The palynological analysis of the core shows three dinoﬂagellate cyst assemblages that have paleoecological signiﬁcance as is illustrated by

Fig. 2, 3andPlate I:

- Between 90 and 75 cm, dinoﬂagellate cysts dominate other organic microfossils (spores, pollen grains, foraminifera chitinous) (75–83%). Within this interval, autotrophic cysts dominate (93–100%) with re-spect to heterotrophic cysts. The inner neritic cyst Lingulodinium machaerophorum is dominant (27 and 40%). Inner neritic cysts of the genus Spiniferites (S. bentorii, S. bulloideus, S. membranaceus, S. hyperacanthus and S. septentrionalis) represent the 5_{–10% of the entire} assemblage. Note Spiniferites lazus is present with relatively high per-centages from 5 to 7%. The oceanic genus Impagidinium, represented by the species I. patulum (4–5%), I. sphaericum I. paradoxum (4–5%) and I. aculeatum(0–2%).

- Between 75 and 15 cm, Lingulodinium machaerophorum is still high reaching 41%. Among the external neritic and oceanic species, Spiniferites lazus disappear, Impagidinium sphaericum and Nematosphaeropsis labyrinthus (3%) decrease in abundance, and re-markable presence of Spiniferites mirabilis (30%) and Impagidinium aculeatum (20%). Heterotrophic dinoﬂagellates develop during this in-terval: Multispinula quanta, (11 and 16%), the genus Brigantedinium (B. caracoense, B. irregulare, B.simplex, B. asymmetricum and Brigantedinium

Fig. 2. Chart illustrating the total count and diversity of the marine palynomorphs, vertical stratigraphic distribution of the recorded dinoﬂagellate cysts per number of cysts counted;in the boxcore MD 13-3441. Age: Coral age (Schröder-Ritzrau et al., 2015), lithofacies: (Terhzaz, 2019).

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ssp from5 to 10%, Lejeunacysta sabrina, between 0 and 5% and the genus Selenopemphix between 0 and 5%.

- Between 15 cm and the surface, autotrophic taxa reach the 80–92%. Lingulodinium machaerophorum remains abundant but is still below the values reached at the base of the previous interval. Additionally, Spiniferites mirabilis and Impagidinium aculeatum reach 30 and 20%, re-spectively. Operculodinium centrocarpum is consistently present with values of 4–6% in previous intervals and decrease in abundance towards the sediment surface (2%). Heterotrophic taxa represented by Multispinula quanta (12%), Brigantedinium (B. cariacoense, B. irregulare, B. simplex, B. asymmetricum and Brigantedinium spp.) display values ﬂuctuating between 0 and 4%, Lejeunacysta sabrina between 1 and 2% and Selenopemphix reaches up to 4%.

3.2.2. Moroccan Mediterranean margin

3.2.2.1. The box core MD13-3465 :. The MD13-3465 boxcore is 60 cm long. Sediments consist of grayish to olive green micritic mud between the base up to 5 cm and brownish muddy allochemic limestone from 5 cm to the surface (Terhzaz et al., 2018). The estimated age of the sed-iments is 9.85 ka at the base and 9.69 ka at the top (Terhzaz et al., 2018). Sediments, therefore, belong to the middle Holocene/Northgrippian. Four samples were analyzed between 30 cm and the surface

The distribution of dinoﬂagellate cysts is relatively homogeneous. The percentage of autotrophic taxa increases from bottom to top, from 47 to 71%. Among them, the cyst typically of internal neritic environ-ment Lingulodinium machaerophorum varies between 10 and 19%. Among neritic Operculodinium centrocarpum cysts have a homogeneous

distribution in the core, between 2 and 5%. The genus Spiniferites is rep-resented by the species S.bulloïdeus, S. bentorii, S. membranaceus, S. septentrionalis and Spiniferites spp. showing values from 2 to 7%, and by S. mirabilis, which is the dominant species. It increases in abundance from 5% at the base, to 35% at the top of the sedimentary sequence. Nematospaheropsis labyrinthus is constantly present but its abundance never exceeds 3%. The oceanic taxa Impagidinium aculeatum increases in abundance from the base (5%) to the top (15%). Impagidinium paradoxum is also present and I. sphaericum is rare. The percentage of heterotrophic taxa decreases towards the top; they are represented in particular by Multispinula qunta (5–19%), Polykrikos kofoïdii (10–17%) and Brigantedinium spp. (5–6%). (Figs. 4 , 5andPlate I)

3.2.2.2. The box core MD13-3456:. The MD13-3456 box core spans 80 cm of sediments. From the base up to 10 cm they consist of gray micritic mud, the top most 10 cm consists of brownish mud (Terhzaz et al., 2018). The age of the sediment was estimated by (Terhzaz et al., 2018) taking into account 500 years between the age of the corals and the surrounding sediment proposed byStalder et al. (2015). The age of the sample taken from the base to 60 cm was estimated 5.9 ka and the samples above, between 10 and 0 cm estimated 5.45 ka. Five sam-ples were taken in this core including two samsam-ples from 10 to 0 cm. They belong to the middle Holocene (Northgrippien) (Walker et al., 2018)

Dinoﬂagellate assemblages are relatively homogeneous; both het-erotrophic and autotrophic taxa display valuesﬂuctuating from 42 to 59%, respectively. Lingulodinium machaerophorum, a taxon characteris-tic of the inner nericharacteris-tic zone shows values from 9 to 19%, with a slight

Fig. 3. Chart illustrating the total count and diversity of the marine and terrestrial palynomorphs, vertical stratigraphic distribution of the recorded pollen, basal foraminifera, Dinoﬂagellates cysts (total number) compared to all the palynological content, Heterotrophic and autotrophic species with the ratio (Heterotrophic/Autotrophic) per number of cysts counted and cold and temperate pollen per number of pollen counted in the boxcore MD 13-3441.

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decrease at the top. Operculodinium centrocarpum abundance values re-main around 2–3%. Spiniferites mirabilis increase in abundance from the bottom to the top of the sedimentary sequence from 5 to 20%, while other species (S. bentorii, S. bulloideus, S. membranaceus, S. septentrionalis) have values from 5 and 8%.

The oceanic species Impagidinium aculeatum display values between 8 and 17%, and it is accompanied mainly by I. sphaericum (2–3%). Het-erotrophic cysts are diversiﬁed: Multispinula quanta present high per-centages between 13 and 25%, Lejeunacysta oliva and Lejeunacysta sabrina (1–3%) appear from 25 cm to the surface, Selenopemphix quanta, S. sp. and S. nephroides (2–4%) decrease in abundance towards the top of the sedimentary succession. Also present are: Polykrikos kofoidii and Polykrikos schwartzii (1–7%) and Trinovantedinium capitatum (3–5%).

(Figs. 6 , 7 and Plate I)

3.2.2.3. The box core MD13-3461:. MD13-3461 boxcore has a thickness of 80 cm and is composed of gray muddy micrite of the base to 15 cm and mud brownish micritic from 15 upward (Terhzaz et al., 2018).

The ages of the sediments are estimated at 6.29 ka, between 60 and 45 cm, and 5.14 ka between 5 and 0 cm (Terhzaz et al., 2018) and there-fore, they belong to the middle Holocene (Northgrippian) (Walker et al., 2018). Five samples were taken from this box core from 80 cm up to the surface.

Dominated by autotrophic cysts, the assemblages are composed by the neritic species Spiniferites bentorii, S. bulloideus, S. membranaceus, S. hyperacanthus, S. delicatus and S. septentrionalis and by oceanic species such as Impagidinium patulum, I. paradoxum, I. sphaericum, Spiniferites mirabilis (external neritic species) and Impagidinium aculeatum are the dominant taxa; and their values ﬂuctuate between 10 and 20%. Operculodinium centrocarpum represents only the 3% of cyst assem-blages. The contribution of Lingulodinium machaerophorum (internal neritic species)ﬂuctuates around 10% but reaches 19% at the top of the sedimentary succession. Heterotrophic taxa are represented by Multispinula quanta (11–17%). (Figs. 8 , 9andPlate I)

3.2.2.4. The box core MD13-3468 :. The box core MD13-3468 has a thick-ness of 40 cm. Sediments consist of grayish micritic mud from 40 to 2 cm and a brownish micritic mud for the upper 2 cm. Between 15 and 5 cm, sediments are dated as old as 10.07 ka (Schröder-Ritzrau et al., 2015) and thus, attributed to the upper Holocene/Meghalayian.

One sample was analyzed at the base of the core and two samples between 10 cm and the surface

The abundances of dinoﬂagellate cysts in these sediments is rather homogeneous, however, autotrophic cysts increase in abundance to-wards the top of the sedimentary succession. Lingulodinium machaerophorum has value ﬂuctuating between 8 and 10%.

Fig. 4. Chart illustrating the total count and diversity of the marine and terrestrial palynomorphs, vertical stratigraphic distribution of the recorded dinoﬂagellate cysts per number of cysts counted in the boxcore MD 13-3465. Age: estimated sediment age (proposed byStalder et al. (2015)), lithofacies: (Terhzaz, 2019).

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Operculodinium centrocarpum has low percentages, between 2 and 4%. Spiniferites mirabilis, display abundances up to 35% while S. bentorii, S bulloideus, S. membranaceus are rarer with values from 4 to 6% of the total. Spiniferites mirabilis is accompanied by Impagidinium aculeatum (11–15%). Also present are Impagidinium paradoxum (3–7%) and Impagidinium patulum (1%). Heterotrophic taxa are represented by Multispinula quanta (7–13%). (Figs. 10 , 11andPlate I)

The microﬂora recorded in our sediments has very low rates: be-tween 17 and 102 taxa, despite this low representativeness, it could be a valuable tool, in parallel with dinoﬂagellate cysts, for assessing cli-matic variations over the study interval. It is constituted by herbaceous and steppe species (Artemisia, Amaranthaceae–Chenopodiaceae, Asteraceae–Cichorioideae and Poaceae), Trees and shrubs (Deciduous Quercus, Evergeen Quercus, Ericaceae and Olea), and altitudinal conifers (Pinus, Cedrus, Abies and Picea).

The MD13-3441 box core (Upper Pleistocene/Tarantian-Middle Ho-locene.) shows three associations listed with a number of taxa between 17 and 68.

-Theﬁrst corresponds to the Tarantian stage (12.09–11.7 ka), shows a dominance of trees and shrubs (67–79%), coupled by altitudinal conifers (15–21%), and the herbaceous and steppe species oscillates between 3 and 12%.

-The second between 11.7 and 10.84 ka. This association displays herbaceous and steppe species (50–67%); followed by trees and shrubs (14–23%) and altitudinal conifers (19–28%).

-The third occurs between 10.84 and 6.8 ka, shows a dominance of trees and shrubs with 59–64%, followed by the altitudinal conifers (21–29%)and ﬁnally herbaceous and steppe species (9–18%). The MD13-3468 and MD13-3465 cores reveals also three types of associations for the lower Holocene (10.07 and 9.69 Ka), contains 61 and 102 of taxa.

-Theﬁrst, is visible around 10.07 ka(MD13-3468), contains 61 pol-len taxa with a dominance of herbaceous and steppe species of about 85%, the trees and shrubs constitutes 12% and altitudinal coni-fers 3%.

-The second association occurs at 9.85 ka (MD13-3465) also domi-nated by herbaceous and steppe species (78%), followed by trees and shrubs (14%), and altitudinal conifers at 8%.

-The third at 9.69 ka (MD13-3465), is slightly different from theﬁrst two associations: herbaceous and steppe species (83%), outrun the trees and shrubs 9%, followed by altitudinal conifers (8%).

From 6.29 to 5.14 ka: two cores: core MD13-3461 (6.29−5.14 ka) and core MD13-3456 (5.9–5.45 ka) are representative of the middle Ho-locene stage.

-The pollen content of the sediments of both cores displays a num-ber of taxa between 35 and 75: 75 taxa in the core MD13-3456 (5.9 ka), 42 in MD13-3456 (5.45 ka), 48 in MD13-3461(5.14 ka) and 35 in MD13-3461 (6.25 ka).

Fig. 5. Chart illustrating the total count and diversity of the marine and terrestrial palynomorphs, vertical stratigraphic distribution of the recorded pollen, basal foraminifera, Dinoﬂagellates cysts (total number) compared to all the palynological content, Heterotrophic and autotrophic species with the ratio (Heterotrophic/Autotrophic) per number of cysts counted and cold and temperate pollen per number of pollen counted in the boxcore MD 13-3465.

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-It shows a dominance of herbaceous and steppe species between 5.9 and 5.14 ka with percentages oscillating between 39 and 67% (MD13-3456) and 75% (MD13-3461). Whereas 35 pollen taxa are dominated by trees and shrubs 57% in MD13-3461 box core (6.29 ka), followed by altitudinal conifers (23%) and then herba-ceous and steppe elements with a percentage of 20%.

3.3. Interpretation and discussion

Palynological analysis of organic residues obtained after treatment with strong acids (HCl and HF) reveals a good richness of the marine fraction (54–90%) compared to pollen grains (10 and 46%), with a clear dominance of dinoﬂagellate cysts (29–85%) (Figs. 3,5,7,9and

11). Despite the low representativeness of pollen grains, they may be a valuable tool, in parallel with dinoﬂagellate cysts, for assessing cli-matic variations over the study interval: Late Pleistocene–Middle Holocene.

For dinoﬂagellate cysts, two groups are distinguished by two oppo-site polarity regarding the temperature (Harland, 1983; Morzadec-Kerfourn, 1984, 1988; Penaud et al., 2009; Rouis-Zargouni, 2010).

- The group of temperate-warm cysts (WT) includes species belonging to the genus Impagidinium (Stover and Evitt, 1978); the species of this genus have a maximal abundance between 40° and 30° north parallel (Harland, 1983; Zonneveld et al., 2013). The most temperate forms are Impagidium patulum, Impagidium paradoxum and Impagidium aculeatum. Most species of genus Impagidinium are presently dominant in warm tropical and warm temperate waters between 20°N and 35°N,

covering a wide range of temperatures (Edwards and Andrle, 1992; Rochon et al., 1999; Marret and Zonneveld, 2003b) and are indicative of an oceanic setting (Harland, 1983; Turon, 1984; Bouimetarhan et al., 2009a). They are accompanied by species belonging to the genus Spiniferites (Mantell et al., 1850): Spiniferites mirabilis, Spiniferites delicatus and Spiniferites membranaceus, which are typical of neritic to oceanic environments (Wall et al., 1977).

- The group of cold-temperate cysts (CT) includes Operculodinium centrocarpum species, a neritic form dominating the continental slope (Morzadec-Kerfourn, 1988). The distribution of this cyst in the surface sediments appears to be associated with the North Atlantic Current (Harland, 1983; Zonneveld et al., 2003;Rouis-Zargouni, 2010). The dis-tribution of this species is observed from polar, equatorial and coastal regions to the open ocean (Rochon, 1997; Zonneveld et al., 2013). It may be abundant in sites where water temperature is higher than 0 °C throughout the year. High relative abundances can be observed in polar areas where salinities are reduced as a result of the melt water input during the summer season or due to the fresh water discharge from rivers. It tolerates a variety of temperature and salinity conditions. However, it is a good indicator of the penetration of North Atlantic warm waters into the Bay of Biscay (Penaud et al., 2008).The Nemathosphearopsis labyrinthus species is a typical oceanic species. Its maximum distribution in the North Atlantic is between 45° and 65° North (Rochon et al., 1999; Marret et al., 2004; de Vernal et al., 2005; Zonneveld et al., 2003). Nematosphaeropsis labyrinthus (Ostenfeld, 1903; Reid, 1974; Zonneveld et al., 2003) is a cosmopolitan species which may be relatively highly abundant in eutrophic as well as oligo-trophic environments. A wide tolerance for sea surface temperatures

Fig. 6. Chart illustrating the total count and diversity of the marine palynomorphs, vertical stratigraphic distribution of the recorded dinoﬂagellate cysts per number of cysts counted in the boxcore MD 13-3456. Age: estimated sediment age (proposed byStalder et al. (2015)), lithofacies: (Terhzaz, 2019).

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ranging from 2.1 to 29.8 °C (Spring–Summer) and 25.8 to 39.4 °C (Sum-mer–Autumn) exist excepted for two sites in the North Atlantic Ocean and the Beaufort Sea where sea surface temperatures vary between 17.4 and 20.2 °C, respectively (Zonneveld et al., 2013b)

Although present in areas where bottom water are anoxic/hypoxic, high relative abundances can be also observed in areas where the sea-ﬂoor is well ventilated. Nematosphaeropsis labyrinthus characterizes oceanic upwelling areas where it dominates the assemblages (Ostenfeld, 1903; Reid, 1974; Zonneveld et al., 2003).

The species Spiniferites lazus is typical of subpolar to temperate re-gions in the North Atlantic. It can be observed in the open sea, coastal sites with high concentrations of nitrates and well-ventilated bottom water (Reid, 1974; Zonneveld et al., 2003).

Heterotrophic dinoﬂagellate tolerate wider variations in salinity and temperature and are more dependent on nutrients (Marret and Zonneveld, 2003a). Moreover, they dominate in upwelling regions per-manent or seasonal (Taylor and Pollingher, 1987; Marret, 1994;

Zonneveld et al., 2001;Radi and Vernal, 2004). They become abundant in presence of high prey availability (diatoms,ﬂagellates, bacteria) (Hansen, 1991; Landry et al., 2000; Grattepanche et al., 2011). Their dominance is also reported in high latitude environments (Rochon et al., 1999). Therefore, heterotrophic dinoﬂagellate are increasingly considered as indirect markers of primary productivity (Wall et al., 1977; Marret, 1994;Dale, 1996;Zonneveld, 1997;Zonneveld et al., 2001;Dale et al., 2002;Sangiorgi et al., 2002; Marret and Zonneveld, 2003b;Sprangers et al., 2004;Susek et al., 2005;Holzwarth et al., 2007;Pospelova et al., 2008).

The sediments from box core MD13-3441 contain abundant late Pleistocene/Tarentien cold taxa. The species Spiniferites lazus, Nematosphaeropsis labyrinthus, Impagidinium sphaericum indicate an

outer neritic to an oceanic environment rich in nutrients (Turon and Londeix, 1988; Devillers and de Vernal, 2000). These species have a dominant latitudinal distribution beyond North 50th parallel.

These cold taxa signiﬁcantly decreasing upward from the Holocene/ Greenlandian. They are replaced by Spiniferites mirabilis and Impagidinium aculeatum in the sediments from the middle Holocene/ Northgrippian. The abundance of Lingulodinium machaerophorum in this box core indicates that the sediments were deposited in an environ-ment rich in nutrients from the continent possibly upwelled from the seaﬂoor (Bouimetarhan et al., 2009; Zonneveld et al., 2013)

In this sedimentary succession, a temporary increase in heterotro-phic cysts indicative of upwelling (Taylor and Pollingher, 1987) suggest that during the lower Holocene upwellings condition characterized the region.

Middle Holocene sediments recovered on the Moroccan Mediterra-nean margin (box core MD13-3461) observe:

- A notable increase in the percentages of Impagidinium aculeatum comparable to that of Spiniferites mirabilis suggesting temperate waters. - Heterotrophic taxa show good development at the base of the core and regress to the top.

The sediments recovered in box core MD13-3456 are middle Holo-cene in age. As in MD13-3461 box core:

- Thermophilic taxons Impagidinium aculeatum and Spiniferites mirabilis are the most dominant.

- Lingulodinium machaerophrum is still present with the abundance of heterotrophic species, which testiﬁes to the contribution of the conti-nent in nutrients.

The sediments recovered in box core MD13-3465 are dated as old as the lower Holocene, between 9.69 and 9.85 ka. The absence of Spiniferites lazus (CT) and the decrease in abundance of the cold taxa

Fig. 7. Chart illustrating the total count and diversity of the marine and terrestrial palynomorphs, vertical stratigraphic distribution of the recorded pollen, basal foraminifera, Dinoﬂagellates cysts (total number) compared to all the palynological content, heterotrophic and autotrophic species with the ratio (Heterotrophic/Autotrophic) per number of cysts counted and cold and temperate pollen per number of pollen counted in the boxcore MD 13-3456.

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Nematosphaeropsis labyrinthus accompanied by the increase in abun-dance of Spiniferites mirabilis and Impagidinium aculeatum (WT) indicate the initial establishment of temperate water conditions. The inﬂuence of neritic input, detected by the presence of Lingulodinium machaerophorum, is relatively modest.

The progressive warming is suggested also by the increasing abun-dances of the autotrophs taxa Spiniferites mirabilis and Impagidinium aculeatum in the Lower Holocene sediments recovered in box core MD13-3468.

The sediments recovered in the southern part of the Alboran Sea also record the installation of the temperate conditions from the lower Holo-cene to middle HoloHolo-cene, during the HoloHolo-cene climatic optimum. In this time interval, inner neritic to oceanic dinoﬂagellate assemblages in-cludes the taxa Spiniferites mirabilis and Impagidinium aculeatum (WT) in equal percentages (Zapata et al., 2013) documented that the lower Holocene in the area of Ifri Oudadane in NE Morocco was characterized by the cyclicity of hot and humid phases. The interval from 11 to 7.6 ka was characterized by a hot-humid climate; the interval from 7.6 to 6.6 ka was characterized by a humid-warm climate, with maximum hu-midity between 7.4 and 6, 6 ka. This was conﬁrmed by the investigation performed on the sediments from box core MD13-3441, MD13-3465 and MD13–3468 in the Atlantic and Mediterranean. In particular, during the Younger Dryas a well known cold period in the Holocene (Barbaza, 2011), the cold water taxon Nematosphaeropsis labyrinthus dominated. Immediately after this cold time, in the middle Holocene, this taxon is replaced by thermophilic taxa such as Impagidinium aculeatum and Spiniferites mirabilis, which suggesting warming.

During the lower Holocene (9.69–9.85 ka) the sedimentary archive recovered in MD 13-3465 box core reveals the existence of semi-arid climatic conditions. This semi-arid climate phase was followed by an arid climate at 10.07 ka box core MD 13-3468 (Terhzaz et al., 2018). The microﬂora, despite its low representativeness, corroborated these results by the predominance of herbaceous and steppe elements (Asteraceae–Cichorioideae, Amaranthaceae–Chenopodiaceae, Artemisia and Poacea) suggests that the continental climate varied between semi-arid (9.85 ka) and arid (9.69 ka), thus indicating a warm temper-ate marine environment and climtemper-ate oscillating between semi-arid to arid around 10.07 ka (MD 13-3468). These results are consistent with those obtained byTerhzaz et al. (2018).

During the middle Holocene (6.29 ka), the palynological data (MD 13-3461) suggest the establishment of a semi-humid climate conﬁrmed by the dominance of tree and shrubs pollen (Deciduous Quercus, Evergeen Quercus, Ericaceae and Olea). This semi-humid climate was followed by a dry warm phase, from 5.45 to 5.14 ka (MD 13-3456 and MD 13-3461) as suggested by the decrease in abundance of cold climate species (trees and shrubs) and by the abundance of herbaceous pollens and steppe species (Asteraceae–Cichorioideae, Amaranthaceae– Chenopodiaceae, Artemisia and Poacea).

The heterotrophic vs. autotrophs can be successfully used to test the climate hypothesis expressed in this research (Fig. 11). This ratio can be used as a proxy for paleotemperature: lower ratio corresponds to warmer waters (Pospelova et al., 2006).

Fletcher (2013)reconstructed the middle Holocene climate for the western Mediterranean and suggested that a dry climate prevailed at

Fig. 8. Chart illustrating the total count and diversity of the marine and terrestrial palynomorphs, vertical stratigraphic distribution of the recorded dinoﬂagellate cysts per number of cysts counted;in the boxcore MD 13-3461. Age: estimated sediment age (proposed byStalder et al. (2015)), lithofacies: (Terhzaz, 2019).

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Fig. 9. Chart illustrating the total count and diversity of the marine and terrestrial palynomorphs, vertical stratigraphic distribution of the recorded pollen, basal foraminifera, Dinoﬂagellates cysts (total number) compared to all the palynological content, Heterotrophic and autotrophic species with the ratio (Heterotrophic/Autotrophic) per number of cysts counted and cold and temperate pollen per number of pollen counted in the boxcore MD13-3461.

Fig 10 Chart illustrating the total count and diversity of the marine and terrestrial palynomorphs vertical stratigraphic distribution of the recorded dinoﬂagellate cysts per number of cysts

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around 5.45 ka. The interpretation of the heterotrophic vs. autotrophs ratio (Fig. 11,Table 2) seems to conﬁrm the assumption ofFletcher (2013)but disagrees withTerhzaz et al. (2018)who suggested semi-arid–subhumid climate during the interval from 6.29 to 5.14 ka. How-ever, unstable environmental conditions during this time, as suggested by evidence of stress in the ostracod species Krithe praetexta (Pirkenseer, 2018) may account for the discrepancy.

4. Conclusion

This work is theﬁrst study on palynology of carbonate mound sedi-ments in the Moroccan Atlantic and Mediterranean margins. The

organic remaining revealed the presence of associations rich in palynomorphs (pollen, dinoﬂagellate cysts, and basal chitinous forami-nifera). Variations in the relative frequencies of the selected taxa (which have a recognized environmental value) allowed the reconstruction of the paleoenvironments during the interval: Terminal Pleistocene– Middle Holocene.

Despite the low representativeness of the continental fraction (spores and pollen) in our organic residues, its contribution remains a valuable tool for the interpretation of climate change.

The dinoflagellate cysts assemblages identified in Pleistocene/ Tarantian sediments (11.7_{–12.09 ka), recovered along the Moroccan} At-lantic margin (box core MD13-3441), contain abundant cold-water taxa, mainly Nemathosphearopsis labyrinthus. This signal has been ob-served in sediments from all the sites in the phase coinciding with the Young Dryas. Heterotrophic taxa also suggest increased marine produc-tivity during this time. The cold assemblage consisting of Spiniferites lazus and Impagidinium sphaericum indicate that the sediments were depos-ited in the external neritic to oceanic areas, in a nutrient-rich environ-ment. The significant presence of pollen from trees and shrubs (Deciduous Quercus, Evergeen Quercus and Ericaceae and Olea) coupled by altitudinal conifers (Pinus, Cedrus, Abies and Picea) confirms that the cold climate prevailed in both the continental and marine environments. The early Holocene (11–7.6 ka) was characterized by the passage from outer neritic to the inner neritic environment and decrease abun-dances of cold taxa. The remarkable appearance of thermophilic taxa such as Spiniferites mirabilis and Impagidinium acculeatum and the estab-lishment of cyclical hot and humid phases. Pollens indicate a climatic os-cillation from arid to humid during this period, whose arid period (11.7–10.84 ka) was characterized by dominance of herbaceous and steppe elements, and the humid period (10.84–6.8 ka) is characterized by dominance of trees and shrubs.

Fig. 11. Chart illustrating the total count and diversity of the marine and terrestrial palynomorphs, vertical stratigraphic distribution of the recorded pollen, basal foraminifera, Dinoﬂagellates cysts (total number) compared to all the palynological content. Heterotrophic and autotrophic species with the ratio (Heterotrophic/Autotrophic) per number of cysts counted and cold and temperate pollen per number of pollen counted in the boxcore MD 13-3468.

Table 2

Species list used in the Atlantic and Mediterranean Moroccan margins.

Autotrophic species Heterotrophic species Achomosphaera andalousiensis Brigantedinium spp Achomosphaera ramulifera Brigantedinium cariacoense Lingulodinium machaerophorum Brigantedinium irregulare Operculodinium centrocarpum Brigantedinium simplex Impagidinium aculeatum Brigantedinium asymmetricum Impagidinium paradoxum Lejeunecysta oliva

Impagidinium patulum Lejeunecysta sabrina Impagidinium sphaericum Multispinula quanta Nematosphaeropsis labyrinthus Polykrikos kofoidii Spiniferites bentorii Polykrikos schwartzii Spiniferites bulloideus Quinquecuspis concreta Spiniferites membranaceus Selenopemphix nephroides Spiniferites hyperacanthus Selenopemphix quanta Spiniferites mirabilis Trinovantedinium capitatum Spiniferites septentrionalis

Spiniferites lazus

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Plate I. Some common specimens from all the boxes cores. Scale bar = 40μm. (a) Spiniferites membranaceus; (b) Spiniferites mirabilis; (c) Spiniferites bentorii; (d) Spiniferites bulloideus; (e) Spiniferites septentrionalis; (f) Lingulodinium machaerophorum; (g) Polykrikos kofoidii; (h) Impagidinium,patulum; (i) Impagidinium sphaericum; (j) Selenopemphix quanta; (k) Nematosphaeropsis labybrinthus; (l) Selenopemphix nephroides.

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During the middle Holocene (6.29–5.14 ka) the thermophilic Spiniferites mirabilis and Impagidinium acculeatum dominated the dino-flagellate cysts assemblages. Their presence coupled with the autotro-phic vs heterotroautotro-phic ratio suggests warmer waters in the marine environment. This, in turn, may reflect an inner neritic to ocean environ-ment with continental climatefluctuating between semi-humid and dry warm climate:

This interval includes: The base (6.29 ka) whose microﬂora domi-nated by trees and shrubs (Deciduous Quercus, Evergeen Quercus, Ericaceae and Olea) reﬂecting a semi-humid climate.

However, the interval between 5.9 and 5.14 ka marking a dry warm climate by the dominance of herbaceous and steppe elements (Asteraceae–Cichorioideae, Amaranthaceae–Chenopodiaceae, Artemisia and Poacea).

Continental climate change seems to have no signiﬁcant impact on the growth and demise of the deep cold-water coral ecosystems, how-ever, the hydrodynamic conditions, nutrient supply and tectonic have a direct impact on these features in the Gulf of Cadiz and Alboran Sea (Terhzaz et al., 2018)

Declaration of Competing Interests

The authors declare that they have no known competingﬁnancial interests or personal relationships that could have appeared to in ﬂu-ence the work reported in this paper.

Acknowledgement

This study was carried out in the frame of the ESF COCARDE European Research Network and the Research Foundation Flanders (FWO) ICA COCARDE project.

The MD194 EUROFLEETS cruise was carried out under Grant Agree-ment n. 228344, with full and duly acknowledged support of IPEV.

The Swiss National Foundation Projects 200020_131829 partially funded the MD194 EUROFLEETS cruise for the recovery of the box-cores.

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